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Alteration of Bacterial Antibiotic Sensitivity After Short-Term Exposure to Diagnostic Ultrasound

AUTHORS

Seyed Mohammad Javad Mortazavi 1 , 2 , * , Leili Darvish 1 , * , Mohammad Abounajmi 3 , Samira Zarei 4 , Tahereh Zare 1 , Mohammad Taheri 5 , Samaneh Nematollahi 6

AUTHORS INFORMATION

1 Department of Medical Physics and Medical Engineering, School of Medicine, Shiraz University of Medical Sciences, Shiraz, IR Iran

2 Department of Radiology, Faculty of ParaMedicine, Hormozgan University of Medical Sciences, Bandar Abbas, IR Iran

3 Department of Radiology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, IR Iran

4 Department of Microbiology, School of Medicine, Bushehr University of Medical Sciences, Bushehr, IR Iran

5 Department of Microbiology, School of Medicine, Kerman University of Medical Sciences, Kerman, IR Iran

6 Department of Biostatistics, School of Medicine, Shiraz University of Medical Sciences, Shiraz, IR Iran

Corresponding Authors:

ARTICLE INFORMATION

Iranian Red Crescent Medical Journal: 17 (11); e26622
Published Online: November 28, 2015
Article Type: Research Article
Received: January 5, 2015
Revised: March 27, 2015
Accepted: April 14, 2015
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Abstract

Background: Many pathogenic bacteria show different levels of antibiotic resistance. Furthermore, a lot of hospital-acquired infections are caused by highly resistant or multidrug-resistant Gram-negative bacteria. According to WHO, patients with drug-resistant infections have higher morbidity and mortality. Moreover, patients infected with bacteria that are resistant to antibiotics considerably consume more healthcare resources.

Objectives: In this study, we explored a physical method of converting drug-resistant bacteria to drug-sensitive ones.

Materials and Methods: This is an in vitro case-control study, performed at the Ionizing and Non-ionizing Radiation Protection Research Center (INIRPRC), Shiraz University of Medical Sciences (SUMS), Shiraz, Iran in 2014. All experiments were carried out using Gram-negative bacteria Klebsiella pneumonia and E. coli and Gram-positive Staphylococcus aureus and Streptococcus group A, isolated from hospitalized patients. The bacterial strains were obtained from the Persian Type Culture Collection, IROST, Iran (Klebsiella pneumonia PTCC 1290) and Bacteriology Department of Shahid Faghihi Teaching Hospital, Shiraz, Iran (E. coli, Staphylococcus aureus, and Streptococcus group A). The bacteria in culture plates were exposed to diagnostic ultrasound using a MyLab70XVG sonography system for 5 minutes. Then, the bacteria were cultured on Mueller-Hinton agar and incubated at 35°C for 18 hours. Finally, antibiotic susceptibility test was performed and the inhibition zone in both control and exposed groups were measured. Three replicate agar plates were used for each test and the inhibition zones of the plates were recorded.

Results: Compared with the results obtained from unexposed bacteria, statistically significant variations of sensitivity to antibiotics were found in some strains after short-term exposure. In particular, we found major differences (making antibiotic-resistant bacteria susceptible or vice versa) in the diameters of inhibition zones in exposed and non-exposed samples of Klebsiella pneumonia and Streptococcus.

Conclusions: This study clearly shows that short-term exposure of microorganisms to diagnostic ultrasonic waves can significantly alter their sensitivity to antibiotics. We believe that this physical method of making the antibiotic-resistant population susceptible can open new horizons in antibiotic therapy of a broad range of diseases, including tuberculosis.

Keywords

Drug Resistance Ultrasound Infection Antibiotics

Copyright © 2015, Iranian Red Crescent Medical Journal. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background

The World Health Organization (WHO) believes that antimicrobial resistance (AMR) is a progressive and serious threat to global public health that endangers the effective prevention and treatment of an ever-increasing range of infections caused by bacteria, parasites, viruses, and fungi. According to WHO, as AMR can be found in all parts of the world, international actions are needed to overcome this problem as new resistance mechanisms emerge and spread globally.

Diagnostic sonography as a very safe, reliable, and economic way to observe various organs of the body (1, 2) uses ultrasound waves in the frequency range of 1 - 20 MHz (however, frequencies up to 50 - 100 MHz have been used experimentally in ultrasound biomicroscopy, a technique used for obtaining high-resolution in vivo imaging of special regions of the body such as the anterior chamber of the eye). The annual number of ultrasound examinations has increased dramatically over the past decade.

The induction of “adaptive response” in bacteria has been already reported (3). Adaptive response can be defined as the induction of repair by pre-exposure to a low level chemical or physical stress. We have previously shown that pre-exposure of living organisms to low levels of ionizing (4-7) or a large dose of non-ionizing radiation (8-12), decrease the detrimental biological effects on these organisms compared to exposure to the large dose alone. Therefore, adaptive response in bacteria can also be observed as the decrease in lethal effects of antibiotics after exposure to a low level physical stress such as short exposure to electromagnetic radiation or ultrasound.

2. Objectives

On the other hand, we have previously shown that pre-exposure of laboratory animals to non-ionizing electromagnetic radiation in radiofrequency (RF) range can induce a survival adaptive response which can be observed as increased resistance to a subsequent Escherichia coli infection (13, 14). Furthermore, over the past years, we have investigated the bio effects of physical stresses such as exposure to ultrasound for enhancing the sensitivity of bacteria to different antibiotics. This study aimed at developing an ultrasound-assisted method for increasing bacterial sensitivity to antibiotics.

3. Materials and Methods
3.1. Isolation and Identification of Isolates

This is an in vitro case-control study, performed at the Ionizing and Non-ionizing Radiation Protection Research Center (INIRPRC), Shiraz University of Medical Sciences (SUMS), Shiraz, Iran in 2014. The bacterial strains were obtained from the Persian Type Culture Collection, IROST, Iran (Klebsiella pneumonia PTCC 1290) and Bacteriology Department of Shahid Faghihi Teaching Hospital, Shiraz, Iran (E. coli, Staphylococcus aureus and Streptococcus group A).

The samples were cultured on blood agar and MacConkey agar for the isolation of microorganism. The culture plates were incubated at 37°C for 24 hours and observed for the presence or absence of visible bacterial growth.

3.2. Antibiotic Susceptibility Tests

We performed the antibiotic susceptibility tests by using the Kirby-Bauer disk diffusion method on Muller-Hinton agar (Figure 1). Drug susceptibility test was performed for nitrofurantoin, nalidixic acid (30 μg), gentamicin (10 μg), sulfamethoxazole, cephalexin, ciprofloxacin (5 μg), and cephalothin for Gram-negative bacteria and vancomycin (30 μg), erythromycin (15 μg), amoxicillin (20 μg), penicillin (10 Units), clindamycin (2 μg), and cefixime (5 μg) for Gram-positive bacteria. All culture media and antibiotic disks were purchased from Merck (Germany) and HiMedia Laboratories (Mumbai, India), respectively. Results for antibiotic susceptibility pattern before and after exposure to ultrasound were recorded and analyzed. The inhibition zone of each plate was recorded as the average of 2 diameters (mm) measured at right angles to one another. Three replicate agar plates were used for each regime. According to the CLSI guidelines (2013), the result were categorized as sensitive, intermediate, and resistance.

Antibiotic Susceptibility Test Performed by Using the Kirby-Bauer Disk Diffusion Method on Muller-Hinton Agar
Figure 1. Antibiotic Susceptibility Test Performed by Using the Kirby-Bauer Disk Diffusion Method on Muller-Hinton Agar
3.3. Ultrasound Apparatus

The bacteria in culture plates were exposed to diagnostic ultrasound using a recently calibrated MyLab70XVG sonography system (EsaoteBiomedicaMyLab70XVG–Genova, Italia). All ultrasound exposures were performed by a 7.5 - 13 MHz linear array probe (type LA523) by an expert radiologist at Shahid Faghihi teaching Hospital, Shiraz, Iran.

3.4. Statistical Methods

The mean diameters of inhibition zones of the 3 replicates in exposed and non-exposed groups were compared using the nonparametric Mann-Whitney test. The significance level was considered at P < 0.05.

4. Results

Findings of this study are summarized in Tables 1 and 2. Compared to the results obtained from unexposed bacteria, statistically significant variations of sensitivity to antibiotics were found in some strains after short-term exposures. Tables 1 and 2 show the mean diameters of the inhibition zones of non-exposed Klebsiella and those exposed to diagnostic ultrasound in PenM, Res H and Doppler modes, respectively. This part of the study showed major differences in the diameters of zones of inhibition in exposed and non-exposed samples of Klebsiella pneumonia and Staphylococcus aureus. In two modes of ultrasound exposure (PenM and Doppler), ultrasonic waves made sensitive Klebsiella pneumonia resistant to cephalexin (P = 0.001). In ResH mode, ultrasound made sensitive Klebsiella pneumonia intermediate resistant to cephalexin (P = 0.011).

Table 1. The Mean Diameters of the Inhibition Zones (mm) of Klebsiella (PTCC: 1290) in Bacteria Exposed to Diagnostic Ultrasound (PEN M and RES H Modes) and Non-Exposed Bacteriaa
AntibioticBacteria Exposed to Diagnostic UltrasoundNon-Exposed BacteriaP Value
Inhibition ZonesbSensitivityInhibition ZonesbSensitivity
PenM Mode
Nitrofurantoin17.67 ± 0.58Sensitive16.34 ± 0.58Intermediate0.047
Nalidixic acid 20.34 ± 0.58Sensitive19.67 ± 0.58Sensitive0.230
Gentamicin14.34 ± 0.58Intermediate14.67 ± 0.58Intermediate0.519
Sulfamethoxazol20.67 ± 0.58Sensitive21.34 ± 0.58Sensitive0.230
Cephalexin10.67 ± 1.15Resistant16.67 ± 0.58Sensitive0.001
Ciprofloxacin19.67 ± 0.58Intermediate20.34 ± 0.58Intermediate0.230
Cephalothin16.67 ± 0.58Intermediate18.34 ± 0.58Sensitive0.024
Res H Mode
Nitrofurantoin17.34 ± 0.58Sensitive16.34 ± 0.58Intermediate0.101
Nalidixic acid 19.34 ± 0.58Sensitive19.67 ± 0.58Sensitive0.519
Gentamicin13.67 ± 0.58Intermediate14.67 ± 0.58Intermediate0.101
Sulfamethoxazol20.34 ± 0.58Sensitive21.34 ± 0.58Sensitive0.101
Cephalexin13.34 ± 1.15Intermediate16.67 ± 0.58Sensitive0.011
Ciprofloxacin17.67 ± 0.58Intermediate20.34 ± 0.58Intermediate0.005
Cephalothin16.34 ± 0.58Intermediate18.34 ± 0.58Sensitive0.013

a(N = 3).

bData are presented as mean ± SD.

Table 2. The Mean Diameters of the Inhibition Zones (mm) of Klebsiella (PTCC: 1290) in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteria a
AntibioticBacteria Exposed to Diagnostic UltrasoundNon-Exposed BacteriaP Value
Inhibition ZonesbSensitivityInhibition ZonesbSensitivity
Nitrofurantoin16.34 ± 0.58Intermediate16.34 ± 0.58Intermediate> 0.999
Nalidixic acid18.34 ± 0.58Intermediate19.67 ± 0.58Sensitive0.047
Gentamicin12.34 ± 0.58Resistant14.67 ± 0.58Intermediate0.008
Sulfamethoxazole17.67 ± 0.58Sensitive21.34 ± 0.58Sensitive0.001
Cephalexin12.34 ± 0.58Resistant16.67 ± 0.58Sensitive0.001
Ciprofloxacin17.34 ± 0.58Intermediate20.34 ± 0.58Intermediate0.003
Cephalothin16.34 ± 0.58Intermediate18.34 ± 0.58Sensitive0.013

a(N = 3).

bData are presented as mean ± SD.

Tables 3 and 4 show the mean diameters of the inhibition zones of non-exposed Staphylococcus epidermidis and those exposed to diagnostic ultrasound in PenM, ResH and Doppler modes, respectively. Again, statistically significant variations of sensitivity to antibiotics were found in Staphylococcus epidermidis after short-term exposure to ultrasound. However, ultrasound was unable to make antibiotic-resistant bacteria susceptible or to make sensitive bacteria, resistant.

Table 3. The Mean Diameters of the Inhibition Zones (mm) of Staphylococcusepidermidis in bacteria Exposed to Diagnostic Ultrasound (PenM and Res H modes) and Non-Exposed Bacteria
AntibioticBacteria Exposed to Diagnostic UltrasoundNon-Exposed BacteriaP Value
Inhibition ZonesaSensitivityInhibition ZonesaSensitivity
Pen M Mode
Vancomycin16.34 ± 0.58Sensitive18.67 ± 0.58Sensitive0.008
Erythromycin9.34 ± 0.58Resistant10.67 ± 0.58Resistant0.047
Amoxicillin14.5 ± 0.5Resistant19.67 ± 0.58Resistant0.0001
Penicillin17.34 ± 0.58Resistant19.67 ± 0.58Resistant0.008
Cefixime9.84 ± 0.77Resistant9.34 ± 0.58Resistant0.417
ResH Mode
Vancomycin16.67 ± 0.58Sensitive18.67 ± 0.58Sensitive0.013
Erythromycin10Resistant10.67 ± 0.58Resistant0.184
Amoxicillin15.5 ± 0.87Resistant19.67 ± 0.58Resistant0.002
Penicillin19.67 ± 0.58Resistant19.67 ± 0.58Resistant> 0.999
Cefixime9.34 ± 0.58Resistant9.34 ± 0.58Resistant> 0.999

aData are presented as mean ± SD.

Table 4. The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus epidermidis in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa
AntibioticBacteria Exposed to Diagnostic UltrasoundNon-Exposed BacteriaP Value
Inhibition ZonesbSensitivityInhibition ZonesbSensitivity
Vancomycin16.34 ± 0.58Sensitive18.67 ± 0.58Sensitive0.008
Erythromycin8.84 ± 0.29Resistant10.67 ± 0.58Resistant0.008
Amoxicillin16.67 ± 0.58Resistant19.67 ± 0.58Resistant0.003
Penicillin19.34 ± 0.58Resistant19.67 ± 0.58Resistant0.519
Cefixime9.34 ± 0.58Resistant9.34 ± 0.58Resistant> 0.999

a(N = 3).

bData are presented as mean ± SD.

Tables 5 and 6 show the mean diameters of the inhibition zones of non-exposed Staphylococcus aureus and those exposed to diagnostic ultrasound in PenM, ResH and Doppler modes, respectively. As observed in previous tests, statistically significant variations of sensitivity to antibiotics were found in Staphylococcus aureus after short-term exposure to ultrasound. In this experiment, ultrasound was able to make antibiotic-resistant bacteria susceptible. In one mode of ultrasound exposure (PenM) ultrasound made resistant Staphylococcus aureus sensitive to amoxicillin (P = 0.003). However, ultrasound was unable to make antibiotic-resistant bacteria susceptible in other modes (ResH and Doppler). Tables 7 and 8 show the mean diameters of the inhibition zones of non-exposed Salmonella sp. and those exposed to diagnostic ultrasound in PenM, ResH and Doppler modes, respectively. Although statistically significant variations of sensitivity to antibiotics were found in Salmonella sp. after short-term exposure to ultrasound, conversion of antibiotic-resistant bacteria to susceptible or vice versa was not found.

Table 5. The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus aureus in Bacteria Exposed to Diagnostic Ultrasound (PenM and ResH Modes) and Non-Exposed Bacteriaa
AntibioticBacteria Exposed to Diagnostic UltrasoundNon-Exposed BacteriaP Value
Inhibition ZonesbSensitivityInhibition ZonesbSensitivity
Pen M Mode
Vancomycin17.67 ± 0.58Sensitive14.67 ± 0.58Sensitive0.003
Erythromycin0Resistant8.34 ± 0.58Resistant0.002
Amoxicillin20.34 ± 0.58Sensitive17.34 ± 0.58Resistant0.003
Penicillin17.67 ± 0.58Resistant13.17 ± 0.77Resistant0.001
Clindamycin29.34 ± 0.58Sensitive26.34 ± 0.58Sensitive0.003
Cefixime15.17 ± 0.29(I)ntermediate16.84 ± 0.29Intermediate0.002
ResH Mode
Vancomycin16.67 ± 0.58Sensitive14.67 ± 0.58Sensitive0.013
Erythromycin0Resistant8.34 ± 0.58Resistant0.002
Amoxicillin17.5 ± 0.87Resistant17.34 ± 0.58Resistant0.795
Penicillin16.67 ± 0.58Resistant13.17 ± 0.77Resistant0.003
Clindamycin29.67 ± 0.58Sensitive26.34 ± 0.58Sensitive0.002
Cefixime15.34 ± 0.58Intermediate16.84 ± 0.29Intermediate0.016

a(N = 3).

bData are presented as mean ± SD.

Table 6. The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus aureus in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa
AntibioticBacteria Exposed to Diagnostic UltrasoundNon-Exposed BacteriaP Value
Inhibition ZonesbSensitivityInhibition ZonesbSensitivity
Vancomycin18.67 ± 0.58Sensitive14.67 ± 0.58Sensitive0.001
Erythromycin0Resistant8.34 ± 0.58Resistant0.002
Amoxicillin18.84 ± 0.29Resistant17.34 ± 0.58Resistant0.016
Penicillin16.34 ± 0.58Resistant13.17 ± 0.77Resistant0.005
Clindamycin29.5 ± 0.87Sensitive26.34 ± 0.58Sensitive0.006
Cefixime15.5 ± 0.5Intermediate16.84 ± 0.29Intermediate0.016

a(N = 3).

bData are presented as mean ± SD.

Table 7. The Mean Diameters of the Inhibition Zones (mm) of Salmonella in Bacteria Exposed to Diagnostic Ultrasound (PEN M and RES H Modes) and Non-Exposed Bacteriaa
AntibioticBacteria Exposed to Diagnostic UltrasoundNon-Exposed BacteriaP Value
Inhibition ZonesbSensitivityInhibition ZonesbSensitivity
PenM Mode
Ciprofloxacin28.34 ± 0.58Sensitive34.34 ± 0.58Sensitive0.0001
Cefixime23.67 ± 0.58Sensitive25.67 ± 0.58Sensitive0.013
Amikacin21.67 ± 0.58Sensitive21.67 ± 0.53Sensitive> 0.999
Sulfamethoxazole/trimethoprim26.67 ± 0.58Sensitive29.67 ± 0.58Sensitive0.003
Cephalexin26.34 ± 0.58Sensitive24.34 ± 0.58Sensitive0.013
Gentamycin20.67 ± 0.58Sensitive20.67 ± 0.58Sensitive> 0.999
ResH Mode
Ciprofloxacin27.34 ± 0.58Sensitive34.34 ± 0.58Sensitive0.0001
Cefixime22.34 ± 0.58Sensitive25.67 ± 0.58Sensitive0.002
Amikacin20.67 ± 0.58Sensitive21.67 ± 0.53Sensitive0.101
Sulfamethoxazole/trimethoprim26.34 ± 0.58Sensitive29.67 ± 0.58Sensitive0.002
Cephalexin23.17 ± 0.29Sensitive24.34 ± 0.58Sensitive0.035
Gentamycin17.67 ± 0.58Sensitive20.67 ± 0.58Sensitive0.003

a(N = 3).

bData are presented as mean ± SD.

Table 8. The Mean Diameters of the Inhibition Zones (mm) of Salmonella in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa
AntibioticBacteria Exposed to Diagnostic UltrasoundNon-Exposed BacteriaP Value
Inhibition ZonesbSensitivityInhibition ZonesbSensitivity
Ciprofloxacin27.67 ± 0.58Sensitive34.34 ± 0.58Sensitive0.0001
Cefixime23.34 ± 0.58Sensitive25.67 ± 0.58Sensitive0.008
Amikacin21.34 ± 0.58Sensitive21.67 ± 0.53Sensitive0.519
Sulfamethoxazole/trimethoprim28.84 ± 0.77Sensitive29.67 ± 0.58Sensitive0.206
Cephalexin23.67 ± 0.58Sensitive24.34 ± 0.58Sensitive0.203
Gentamycin18.5 ± 0.5Sensitive20.67 ± 0.58Sensitive0.008

a(N = 3).

bData are presented as mean ± SD.

5. Discussion

To the best of our knowledge this is the first study that explores the effect of ultrasound exposure as a mechanical stress on the antibiotic susceptibility of some microorganisms. In this study, we found some major alterations in the diameters of the inhibition zones in Klebsiella pneumonia and Staphylococcus aureus after exposure to ultrasound waves. Interestingly, ultrasound was capable of making some antibiotic-resistant bacteria susceptible as well as making some sensitive bacteria, resistant. Antibiotic resistance can be defined as the ability of microorganisms to resist the lethal effects of specific antibiotics. This phenomenon occurs when the effectiveness of drugs to cure or prevent infections reduces or vanishes (15). Lattimer et al. (16) in a paper published in JAMA in 1961 reported that in spite of great advances in medicine, scientists are losing the battle against drug resistance. At that time, they believed that the speed of discovery and development of new drugs was not fast enough to take over the significant ability of some microorganisms to develop resistant mutants. Therefore, they predicted that humans might encounter lethal epidemics in the future if they could not control drug-resistant microorganisms (16). Now, we should confess that the situation has not changed significantly since the publication of this paper more than 50 years ago.

The decrease observed in the diameters of the inhibition zones in Klebsiella pneumonia and Staphylococcus aureus after exposure to ultrasound waves, can be interpreted as an adaptive response. Adaptive response can be defined as the acquisition of radiation resistance against exposure to high dose in cultured cells or organisms which had been previously pretreated with an adapting low dose radiation (this low dose radiation is also called “priming dose” or “conditioning dose”) (17). This observation is generally in line with our previous reports on the induction of adaptive response after exposure to low levels of ionizing (4-7) and non-ionizing radiation (8-12). More specifically, our findings are in line with the reports indicating that when bacteria are exposed to mild forms of different stresses (chemical and physical stresses), this stress improves their abilities to adapt and become resistant to any subsequent more extreme exposures (18-20). Also, that pre-exposure can increase the resistance to other exposures (e.g. exposure to antibiotics) and induce “cross-protection” phenomenon (3).

The main limitation of our experiment was the low number of bacterial strains studied. However, the unique inter-department collaboration in our study was a significant strength point. Based on these results, we believe that short-term exposure of microorganisms to diagnostic ultrasonic waves can significantly alter their sensitivity to antibiotics. It can be concluded that the physical methods of making the antibiotic-resistant population susceptible can open new horizons in antibiotic therapy fora broad range of diseases, including tuberculosis. On the other hand, when exposure to ultrasound makes the antibiotic-susceptible population resistant, this may endanger patients’ lives.

Footnotes
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